Spatial representation of hydrocarbon odorants in the ventrolateral zones of the rat olfactory bulb.

The glomerular sheet of the olfactory bulb (OB) forms odorant receptor maps that are parceled into zones. We previously reported the molecular receptive range (MRR) property of individual glomeruli in the dorsal zone (zone 1) of the OB and showed that polar functional groups play a major role in activating glomeruli in this zone. However, the MRR property of glomeruli in zones 2-4 is not well understood yet. Using the method of intrinsic signal imaging, we recorded odorant-induced glomerular activity from the ventrolateral surface (zones 2-4) of rat OB. While hydrocarbon odorants that lack polar functional groups activate only a few glomeruli in zone 1, we found that a series of hydrocarbon odorants consistently activated many glomeruli in the ventrolateral surface. The hydrocarbon-responsive glomeruli were grouped into two clusters; glomeruli in one cluster (cluster H) responded to benzene-family hydrocarbons but not to cyclic terpene hydrocarbons. Glomeruli in the other cluster (cluster I) responded to both classes of hydrocarbons. Detailed analyses of MRR properties of individual glomeruli using hydrocarbon odorants and polar-functional-group-containing odorants showed that the common and characteristic molecular features effective in activating glomeruli in the clusters H and I are the hydrocarbon skeleton. These results suggest that ORs represented by glomeruli in these clusters recognize primarily the hydrocarbon skeleton of odorants, and thus imply a systematic difference in the manner of recognizing odorant molecular features between ORs in zone 1 and ORs in zones 2-4.

[1]  S. Firestein,et al.  The olfactory receptor gene superfamily of the mouse , 2002, Nature Neuroscience.

[2]  T. Sendera,et al.  Morphometry of rat olfactory bulbs stained for cytochrome oxidase reveals that the entire population of glomeruli forms early in the neonatal period. , 1993, Brain research. Developmental brain research.

[3]  G. Shepherd,et al.  Functional organization of rat olfactory bulb analysed by the 2‐deoxyglucose method , 1979, The Journal of comparative neurology.

[4]  M. Groudine,et al.  Conservation of sequence and structure flanking the mouse and human β-globin loci: The β-globin genes are embedded within an array of odorant receptor genes , 1999 .

[5]  Fahmeed Hyder,et al.  Odor maps of aldehydes and esters revealed by functional MRI in the glomerular layer of the mouse olfactory bulb , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[6]  M. Leon,et al.  Odorant molecular length: One aspect of the olfactory code , 2000, The Journal of comparative neurology.

[7]  Gustavo Glusman,et al.  The complete human olfactory subgenome. , 2001, Genome research.

[8]  Shin Nagayama,et al.  Molecular‐feature domains with posterodorsal–anteroventral polarity in the symmetrical sensory maps of the mouse olfactory bulb: mapping of odourant‐induced Zif268 expression , 2002, The European journal of neuroscience.

[9]  T. Brierley,et al.  A functional map in rat olfactory epithelium. , 1999, Chemical senses.

[10]  Matt Wachowiak,et al.  In Vivo Imaging of Neuronal Activity by Targeted Expression of a Genetically Encoded Probe in the Mouse , 2004, Neuron.

[11]  M. Alenius,et al.  Differential function of RNCAM isoforms in precise target selection of olfactory sensory neurons , 2003, Development.

[12]  L. Buck,et al.  Combinatorial Receptor Codes for Odors , 1999, Cell.

[13]  Dietmar Krautwurst,et al.  Identification of Ligands for Olfactory Receptors by Functional Expression of a Receptor Library , 1998, Cell.

[14]  R G Shulman,et al.  Assessment and discrimination of odor stimuli in rat olfactory bulb by dynamic functional MRI. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[15]  J. Scott,et al.  Chemical Determinants of the Rat Electro-Olfactogram , 2000, The Journal of Neuroscience.

[16]  K. Mori,et al.  Two mirror‐image sensory maps with domain organization in the mouse main olfactory bulb , 2000, Neuroreport.

[17]  H. Breer,et al.  A novel brain receptor is expressed in a distinct population of olfactory sensory neurons , 2000, The European journal of neuroscience.

[18]  H. Sakano,et al.  Olfactory Neurons Expressing Closely Linked and Homologous Odorant Receptor Genes Tend to Project Their Axons to Neighboring Glomeruli on the Olfactory Bulb , 1999, The Journal of Neuroscience.

[19]  H Breer,et al.  Local Permutations in the Glomerular Array of the Mouse Olfactory Bulb , 2000, The Journal of Neuroscience.

[20]  Naoshige Uchida,et al.  Odor maps in the mammalian olfactory bulb: domain organization and odorant structural features , 2000, Nature Neuroscience.

[21]  M. Mezler,et al.  Characteristic features and ligand specificity of the two olfactory receptor classes from Xenopus laevis. , 2001, The Journal of experimental biology.

[22]  Michael Leon,et al.  Functional mapping of the rat olfactory bulb using diverse odorants reveals modular responses to functional groups and hydrocarbon structural features , 2002, The Journal of comparative neurology.

[23]  L. Astic,et al.  Spatial distribution of [14C]2-deoxyglucose uptake in the olfactory bulbs of rats stimulated with two different odours , 1980, Brain Research.

[24]  Shin Nagayama,et al.  Detection and Masking of Spoiled Food Smells by Odor Maps in the Olfactory Bulb , 2004, The Journal of Neuroscience.

[25]  T. Bonhoeffer,et al.  Tuning and Topography in an Odor Map on the Rat Olfactory Bulb , 2001, The Journal of Neuroscience.

[26]  Shuichi Hirono,et al.  Topographic representation of odorant molecular features in the rat olfactory bulb. , 2004, Journal of neurophysiology.

[27]  K. Imamura,et al.  Coding of odor molecules by mitral/tufted cells in rabbit olfactory bulb. I. Aliphatic compounds. , 1992, Journal of neurophysiology.

[28]  K. Mori,et al.  The olfactory bulb: coding and processing of odor molecule information. , 1999, Science.

[29]  W. Precht.  The synaptic organization of the brain G.M. Shepherd, Oxford University Press (1975). 364 pp., £3.80 (paperback) , 1976, Neuroscience.

[30]  K. Mori,et al.  Coding of odor molecules by mitral/tufted cells in rabbit olfactory bulb. II. Aromatic compounds. , 1992, Journal of neurophysiology.

[31]  L. C. Katz,et al.  Optical Imaging of Odorant Representations in the Mammalian Olfactory Bulb , 1999, Neuron.

[32]  H. Breer,et al.  Olfactory receptors in aquatic and terrestrial vertebrates , 1998, Journal of Comparative Physiology A.

[33]  L. Buck,et al.  The Molecular Architecture of Odor and Pheromone Sensing in Mammals , 2000, Cell.

[34]  H. Hayashi,et al.  OCAM: A New Member of the Neural Cell Adhesion Molecule Family Related to Zone-to-Zone Projection of Olfactory and Vomeronasal Axons , 1997, The Journal of Neuroscience.

[35]  Gordon M. Shepherd,et al.  The Olfactory Bulb , 1988 .